2005, Number 3
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Vet Mex 2005; 36 (3)
Cortisol in saliva, urine, and feces: non-invasive assessment of wild mammals
Brousset Hernández-Jáuregui DM, Galindo MF, Valdez PRA, Romano PM, Schuneman AA
Language: English/Spanish
References: 170
Page: 225-237
PDF size: 436.48 Kb.
ABSTRACT
Glucocorticoid evaluation from samples obtained by non-invasive means has opened the possibility of carrying out these determinations in different species of wild mammals, facilitating studies on stress and the impact produced by different stimuli. A proportion of steroid hormones can appear in saliva and they are all metabolized to be eliminated through urine or feces, generally as conjugated or as non-conjugated metabolites, respectively. Nevertheless, the route of excretion and the type of metabolites could change depending on the species, making it necessary to validate the test in each case. The assessment of these steroids could be done through immunoanalysis tests such as radioimmunoassay (RIA), enzyme immunoassay (EIA) and enzyme-linked immunosorbent assay (ELISA). This longitudinal evaluation has been used to evaluate the impact of different types of management, the introduction of new animals, environmental manipulation, transport, translocation, veterinary procedures and assisted reproduction techniques.
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Wingfield JC, Hunt K, Breuner C, Dunlap K, Fowler GS, Freed L, et al. Environmental stress, field endocrinology and conservation biology. In: Clemmons JR, Buchkolz editors. Behavioral approaches to Conservation in the wild. Cambridge: University Press, UK; 1997: 95-131.
W3. asser SK, Hunt KE, Brown JL, Cooper K, Crockett CM, Bechert U, et al. A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Endocrinology 2000; 120: 260-275.
Dantzer R, Mormede P. Stress in farm animals: a need for reevaluation. J Anim Sci 1983; 57:6-18.
Knol BW. Stress and the endocrine hypothalamus-pituitary-testis system: a review. Vet Q 1991; 13:104-114.
Rivier C, Rivest S. Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: peripheral and central mechanism; a review. Biol Reprod 1991; 45:523-532.
Stratakin CA, Chrousos GP. Neuroendocrinology and pathophysiology of the stress system. In Stress, basic mechanism and clinical implications. Ann N Y Acad S 1995; (771): 1-18.
Moodie EM, Chamove AS. Brief threatening events beneficial for captive tamarins? Zoo Biol 1990; 9:275-286.
Wingfield JC, Ramenofsky M. Hormones and the behavioral ecology of stress. In: Balm PHM, editor. Stress physiology in animals. England Sheffield Academic Press-CRC Press; 1999:1-41.
Axelrod J, Reisine TD. Stress hormones: their interaction and regulation. Science 1984; 224:452-459.
Friend TH. Symposium response of animals to stress: behavioral aspects of stress. J Dairy Sci 1991; 74:292-303.
Kopin IJ. Definitions of stress and sympathetic neuronal response. In Stress, basic mechanism and clinical implications; Ann N Y Acad Sci, 1995; 771:19-30.
Clark JD, Rager DR, Calpin JP. Animal well-being III. Specific assessment criteria. Lab Anim Sci 1997b; 47: 586-596.
Guyton AC. Textbook of medical physiology. 8th ed Philadelphia: WB Saunders Co, 1991.
Broom DM, Johnson KG. Assessing welfare: short term responses. In: Broom DM, Johnson KG, editors. Stress and animal welfare, London: Chapman and Hall, 1993:87-144.
Broom DM. The scientific assessment of animal welfare. Appl Anim Behav Sci 1988; 20:5-19.
Moberg GP. Problems defining stress and distress in animals. J Am Vet Assoc 1987; 191:1207-1211.
Rushen J. Problems associated with the interpretation of physiological data in the assessment of animal welfare. App Anim Behav Sci 1991; 28:381-386.
Clark JD, Rager DR, Calpin JP. Animal well-being III. An overview of assessment. Lab Anim Sci 1997a ; 47: 580-585.
Strier KB, Ziegler TE, Wittwer DJ. Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoids). Horm Behav 1999; 35:125-134.
Bélanger B, Couture J, Caron S, Boudou P, Fiet J, Bélanger A. Production and secretion of C19 steroids by rat and guinea pig adrenals. Steroids 1990; 55:360-365.
Brownie AC. The metabolism of adrenal cortical steroids. In: James VHT, editor. The adrenal gland. New York: Raven Press Ltd; 1992: 209-224.
Setchel KDR, Gontscharow NP, Axelson M, Sjövall J. The characterization of polar corticosteroids in the urine of the macaque monkey (Macaca fascicularis) and the baboon (Papio hamadryas). Acta Endocrinol 1975; 79:535-550.
Munck A, Guyre PM, Holbrook NJ. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr Rev 1984; 5:25-44.
Vylitová M, Miksik I, Pácha J. Metabolism of corticosteron in mammalian and avian intestine. Gen Comp Endocrinol 1998; 109:315-324.
Shille VM, Haggerty MA, Shackleton C, Lasley BL. Metabolites of estradiol in serum, bile, intestine and feces of the domestic cat (Felis catus). Theriogenology 1990; 34:779-794.
Senciall IR, Rahal S, Roberts R. Corticosteroid side chain oxidation and metabolism of 20-dihydro steroids and evidence for steroid acid formation by direct oxidation at C-21. J Steroid Biochem Mol Biol 1992; 41:151-160.
Han A, Marandici A, Monder C. Metabolism of corticosterone in the mouse, identification of 11, 20 -dihydroxy-3-oxo-4-pregnen-21-oii acid as a major metabolite. J Biol Chem 1983; 258:13703-13707
Quinkler M, Kosmale B, Bahr V, Oelkers W, Diederich S. Evidence for isoforms of 11 -hydroxysteroid dehydrogenase in the liver and kidney of the guinea pig. J Endocrinol 1998; 153:291-298.
Palme R, Möstl E, Brem G, Schellander K, Bamberg E. Faecal metabolites of infused 14C progesterone in domestic livestock. Reprod Domestic Anim 1997; 32:199-201.
Graham LH, Brown JL. Cortisol metabolism in the domestic cat and implications for noninvasive monitoring of adrenocortical function in endangered felids. Zoo Biol 1996; 15:71-82.
Bahr NI, Palme R, Mohle JK, Heistermann M. Comparative aspects of the metabolism of cortisol in three individual nonhuman primates. Gen Comp Endocrinol 2000; 117:427-438.
Setchel KDR, Shackleton CHL. The in vivo metabolism of cortisol and corticosterone by the macaque monkey (Macaca fascicularis). Acta Endocrinol 1973; 78:91-109.
Gimpel J, Lord A. Validation of faecal corticosteroid analysis. Proceedings of the International Society of Applied Ethology. 2000 Oct 17-20 Florianopolis, Brasil; Ramos A, Pinheiro MLC, Hötzel MJ, editors, Florianopolis; Brasil: Federal University of Santa Catarina, 2000: 137.
Teskey-Gerstl A, Bamberg E, Steineck T, Palme R. Excretion of corticosteroids in urine and feces of hares (Lepus europaeus). J Comp Physiol 2000; 170:163-168.
Schatz S, Palme R. Measurement of faecal cortisol metabolites in cats and dogs: a non-invasive method for evaluating adrenocortical function. Vet Res Commun 2001; 25:271-287.
Restrepo A, Armario A. Chronic stress alters pituitary-adrenal function in prepuberal male rats. Psychoneuroendocrinology 1987; 12:393-398.
Dantzer R. Animal welfare methodology and criteria. Rev Sci Tech 1994; 13:291-302.
Wildt DE. Male reproduction: assessment, management and control of fertility. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S, editors. Wild mammals in captivity. Chicago, Chicago Press; 1996:429-450.
Schiewe MC, Bush M, de Vos V, Brown JL, Wildt DE. Semen characteristics, sperm freezing and endocrine profiles in free-ranging wildebeest (Connochaetes taurinus) and greater kudu (Tragelaphus strepsiceros) J Zoo Wildl Med 1991; 22:58-72.
Goyman W, Möstl E, van’t Hof T, East ML, Hofer H. Non-invasive fecal monitoring of glucocorticoides in spotted hyaenas Crocuta crocuta. Gen Comp Endocrinol 1999; 114:340-348.
Terio KA, Citino SB, Brown JL. Fecal cortisol metabolism analysis for noninvasive monitoring of adrenocortical function in the cheetah (Acinonyx jubatus) J Zoo Wildl Med 1999; 30:484-491.
Stillwell HJ, Brown JL, Graham LH. Assessment of a commercially available radioimmunoassay for the detection of fecal cortisol metabolites in several non domestic felid species. Proceedings of the American Association of Zoo Veterinarians; 1996 November 3-8; Puerto Vallarta, Mexico. St Louis Missouri USA: Charlotte Kirk editor, AZV-AZCARM: 1996: 582-583.
Sapolsky RM. Individual differences in cortisol secretory patterns in the wild baboon: role of negative feedback sensitivity. Endocrinology 1983; 113:2263-2267.
Friend TH, Polan CE, Gwazdauskas FC, Heald CW. Adrenal glucocorticoid response to exogenous adrenocorticotropin mediated by density and social disruption in lactating cows. J Dairy Sci 1977; 60:1958-1963.
Nogueira GP, Silva JCR. Plasma cortisol levels in captive wild felines after chemical restraint. Braz J Med Biol Res 1997; 30:1359-1361.
Morton DJ, Anderson E, Foggin CM, Kock MD, Tiran EP. Plasma cortisol as an indicator of stress due to capture and translocation in wildlife species. Vet Rec 1995; 136:60-63.
Brown JL, Goodrowe KL, Simmons LG, Armstrong DL, Wildt DE. Evaluation of the pituitary-gonadal response to GnRH, and adrenal status in the leopard (Panthera pardus japonensis) and tiger (Panthera tigris). J Reprod Fertil 1988; 82:227-236.
Aubin DJ, Ridgway SH, Wells RS, Rhinehart H. Dolphin thyroid and adrenal hormones: circulating levels in wild and semidomesticated Tursiops truncatus, and influence of sex, age and season. Marine Mammal Sci 1996; 12:1-13.
Parrot RF, Misson BH, Baldwin BA. Salivary cortisol in pigs following adrenocorticotrophic hormone stimulation: comparison with plasma levels. Br Vet J 1989; 145:362-366.
De Jong IC, Prelle IT, Van de Burgwal JA, Lambooij E, Korte SM, Blokhuis HJ, et al. Effects of environmental enrichment on behavioral responses to novelty, learning and memory, and the circadian rhythm in cortisol in growing pigs. Physiol Behav 2000; 68:571-578.
Lutz CK, Tiefenbacher S, Jorgensen MJ, Meyer JS, Novak MA. Techniques for collecting saliva from awake, unrestrained, adult rhesus monkeys for cortisol assay. Am J Primatol 2000; 52:93-99.
Hodges JK. Determining and manipulating female reproductive parameters. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S, editors. Wild mammals in captivity, principles and techniques. Chicago: The University of Chicago Press; 1996; 418-428.
Lasley, BL. Methods for evaluating reproductive function in exotic species. Adv Vet Sci Comp Med 1985; 30: 209-228.
Goossens MMC, Meyer HP, Voorhout G, Sprang EPM. Urinary excretion of glucocorticoids in the diagnosis of hyperadrenocorticism in cats. Dom Anim Endocrinol 1995; 12:355-362.
Korhonen H, Niemela P, Jauhiainen L, Tupasela T. Effects of space allowance and earthen floor on welfare-related physiological and behavioural responses in male blue foxes. Physiol Behav 2000; 69:571-580.
Crockett CM, Shimoji M, Bowden DM. Behavior, appetite and urinary cortisol responses by adult female pigtailed and longtailed macaques to cage size, cage level, room changes and sedation. Am J Primatol 2000; 52:63-80.
Carlstead K, Brown JL, Monfort SL, Killens R, Wildt DE. Urinary monitoring of adrenal responses to psychological stressors in domestic and nondomestic felids. Zoo Biol 1992; 11:165-176.
Bahr NI, Pryce CR, Dobeli M, Martin RD. Evidence from urinary cortisol that maternal behavior is related to stress in gorillas. Physiol Behav 1998; 64:429-437.
Carlstead K, Brown JL, Seidensticker J. Behavioral and adrenocortical responses to environmental changes in leopard cats (Felis bengalensis). Zoo Biol 1993; 12:321-331.
Palme R, Fischer P, Schildorfer H, Ismail MN: Excretion of infused 14C-steroid hormones via feces and urine in domestic livestock. Anim Reprod Sci 1996; 43:43-63.
Adams NR, Abordi JA, Briegel JR, Sanders MR. Effect of diet on the clearance of estradiol-17 in the ewe. Biol Reprod 1994; 51:668-674.
Wasser SK, Thomas R, Nair PP, Guidry C, Southers J, Lucas J, et al. Effects of dietary fiber on faecal steroid measurements in baboons (Papio cynocephalus cynocephalus). J Reprod Fertil 1993; 97:569-574.
McLeod PJ, Moger WH, Ryon J, Gadbois S, Fentress JC. The relation between urinary cortisol levels and social behavior in captive timber wolves. Can J Zool 1996; 74:209-216.
Morais, RN, Mucciolo RG, Gomes ML, Lacerda O, Moraes W, Moreira N, et al. Adrenal activity assessed by fecal corticoids and male reproductive traits in three South American felid species. Proceedings of the American Association of Zoo Veterinarians; 1996 November 3-8; Puerto Vallarta, Mexico. St Louis Missouri USA: Charlotte Kirk editor, AZV-AZCARM: 1996: 220-223.
Jurke MH, Czekala NM, Lindburg DG, Millard SE. Fecal corticoid metabolite measurement in the cheetah (Acinonyx jubatus). Zoo Biol 1997; 16:133-147.
Wallner B, Möstl E, Dittami J, Prossinger H. Fecal glucocorticoids document stress in female Barbary machaques (Macaca sylvanus). Gen Comp Endocrinol 1999; 113:80-86.
Möstl E, Palme R. Hormones as indicators of stress. Dom Anim Endocrinol 2002; 23:67-74
Creel S. Social dominance and stress hormones. Ecol Evol 2001; 16:491-497.
Schwarzenberger F, Kolter L, Zimmermann W, Rietschel W, Matern B, Bircher, P et al. Faecal cortisol metabolite measurement in the okapi (Okapia johnstoni). Proceedings of the 2nd International Symposium on Physiology and Ethology of Wild and Zoo Animals Hofer H editor, Institute of Zoo and Wildlife Research, Berlin 1998, Oct 7-10.
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Brown JL, Wildt DE. Assessing reproductive status in wild felids by noninvasive faecal steroid monitoring. Int Zoo Yb 1997; 35:173-191.
Wingfield JC, Hunt K, Breuner C, Dunlap K, Fowler GS, Freed L, et al. Environmental stress, field endocrinology and conservation biology. In: Clemmons JR, Buchkolz editors. Behavioral approaches to Conservation in the wild. Cambridge: University Press, UK; 1997: 95-131.
Wasser SK, Hunt KE, Brown JL, Cooper K, Crockett CM, Bechert U, et al. A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Endocrinology 2000; 120: 260-275.
Dantzer R, Mormede P. Stress in farm animals: a need for reevaluation. J Anim Sci 1983; 57:6-18.
Knol BW. Stress and the endocrine hypothalamus-pituitary-testis system: a review. Vet Q 1991; 13:104-114.
Rivier C, Rivest S. Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: peripheral and central mechanism; a review. Biol Reprod 1991; 45:523-532.
Stratakin CA, Chrousos GP. Neuroendocrinology and pathophysiology of the stress system. In Stress, basic mechanism and clinical implications. Ann N Y Acad S 1995; (771): 1-18.
Moodie EM, Chamove AS. Brief threatening events beneficial for captive tamarins? Zoo Biol 1990; 9:275-286.
Wingfield JC, Ramenofsky M. Hormones and the behavioral ecology of stress. In: Balm PHM, editor. Stress physiology in animals. England Sheffield Academic Press-CRC Press; 1999:1-41.
Axelrod J, Reisine TD. Stress hormones: their interaction and regulation. Science 1984; 224:452-459.
Friend TH. Symposium response of animals to stress: behavioral aspects of stress. J Dairy Sci 1991; 74:292-303.
Kopin IJ. Definitions of stress and sympathetic neuronal response. In Stress, basic mechanism and clinical implications; Ann N Y Acad Sci, 1995; 771:19-30.
Clark JD, Rager DR, Calpin JP. Animal well-being III. Specific assessment criteria. Lab Anim Sci 1997b; 47: 586-596.
Guyton AC. Textbook of medical physiology. 8th ed Philadelphia: WB Saunders Co, 1991.
Broom DM, Johnson KG. Assessing welfare: short term responses. In: Broom DM, Johnson KG, editors. Stress and animal welfare, London: Chapman and Hall, 1993:87-144.
Broom DM. The scientific assessment of animal welfare. Appl Anim Behav Sci 1988; 20:5-19.
Moberg GP. Problems defining stress and distress in animals. J Am Vet Assoc 1987; 191:1207-1211.
Rushen J. Problems associated with the interpretation of physiological data in the assessment of animal welfare. App Anim Behav Sci 1991; 28:381-386.
Clark JD, Rager DR, Calpin JP. Animal well-being III. An overview of assessment. Lab Anim Sci 1997a; 47:580-585.
Strier KB, Ziegler TE, Wittwer DJ. Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoids). Horm Behav 1999; 35:125-134.
Bélanger B, Couture J, Caron S, Boudou P, Fiet J, Bélanger A. Production and secretion of C19 steroids by rat and guinea pig adrenals. Steroids 1990; 55:360-365.
Brownie AC. The metabolism of adrenal cortical steroids. In: James VHT, editor. The adrenal gland. New York: Raven Press Ltd; 1992: 209-224.
Setchel KDR, Gontscharow NP, Axelson M, Sjövall J. The characterization of polar corticosteroids in the urine of the macaque monkey (Macaca fascicularis) and the baboon (Papio hamadryas). Acta Endocrinol 1975; 79:535-550.
Munck A, Guyre PM, Holbrook NJ. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr Rev 1984; 5:25-44.
Vylitová M, Miksik I, Pácha J. Metabolism of corticosteron in mammalian and avian intestine. Gen Comp Endocrinol 1998; 109:315-324.
Shille VM, Haggerty MA, Shackleton C, Lasley BL. Metabolites of estradiol in serum, bile, intestine and feces of the domestic cat (Felis catus). Theriogenology 1990; 34:779-794.
Senciall IR, Rahal S, Roberts R. Corticosteroid side chain oxidation and metabolism of 20-dihydro steroids and evidence for steroid acid formation by direct oxidation at C-21. J Steroid Biochem Mol Biol 1992; 41:151-160.
Han A, Marandici A, Monder C. Metabolism of corticosterone in the mouse, identification of 11, 20 -dihydroxy-3-oxo-4-pregnen-21-oii acid as a major metabolite. J Biol Chem 1983; 258:13703-13707
Quinkler M, Kosmale B, Bahr V, Oelkers W, Diederich S. Evidence for isoforms of 11 -hydroxysteroid dehydrogenase in the liver and kidney of the guinea pig. J Endocrinol 1998; 153:291-298.
Palme R, Möstl E, Brem G, Schellander K, Bamberg E. Faecal metabolites of infused 14C progesterone in domestic livestock. Reprod Domestic Anim 1997; 32:199-201.
Graham LH, Brown JL. Cortisol metabolism in the domestic cat and implications for noninvasive monitoring of adrenocortical function in endangered felids. Zoo Biol 1996; 15:71-82.
Bahr NI, Palme R, Mohle JK, Heistermann M. Comparative aspects of the metabolism of cortisol in three individual nonhuman primates. Gen Comp Endocrinol 2000; 117:427-438.
Setchel KDR, Shackleton CHL. The in vivo metabolism of cortisol and corticosterone by the macaque monkey (Macaca fascicularis). Acta Endocrinol 1973; 78:91-109.
Gimpel J, Lord A. Validation of faecal corticosteroid analysis. Proceedings of the International Society of Applied Ethology. 2000 Oct 17-20 Florianopolis, Brasil; Ramos A, Pinheiro MLC, Hötzel MJ, editors, Florianopolis; Brasil: Federal University of Santa Catarina, 2000: 137.
Teskey-Gerstl A, Bamberg E, Steineck T, Palme R. Excretion of corticosteroids in urine and feces of hares (Lepus europaeus). J Comp Physiol 2000; 170:163-168.
Schatz S, Palme R. Measurement of faecal cortisol metabolites in cats and dogs: a non-invasive method for evaluating adrenocortical function. Vet Res Commun 2001; 25:271-287.
Restrepo A, Armario A. Chronic stress alters pituitary-adrenal function in prepuberal male rats. Psychoneuroendocrinology 1987; 12:393-398.
Dantzer R. Animal welfare methodology and criteria. Rev Sci Tech 1994; 13:291-302.
Wildt DE. Male reproduction: assessment, management and control of fertility. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S, editors. Wild mammals in captivity. Chicago, Chicago Press; 1996:429-450.
Schiewe MC, Bush M, de Vos V, Brown JL, Wildt DE. Semen characteristics, sperm freezing and endocrine profiles in free-ranging wildebeest (Connochaetes taurinus) and greater kudu (Tragelaphus strepsiceros) J Zoo Wildl Med 1991; 22:58-72.
Goyman W, Möstl E, van’t Hof T, East ML, Hofer H. Non-invasive fecal monitoring of glucocorticoides in spotted hyaenas Crocuta crocuta. Gen Comp Endocrinol 1999; 114:340-348.
Terio KA, Citino SB, Brown JL. Fecal cortisol metabolism analysis for noninvasive monitoring of adrenocortical function in the cheetah (Acinonyx jubatus) J Zoo Wildl Med 1999; 30:484-491.
Stillwell HJ, Brown JL, Graham LH. Assessment of a commercially available radioimmunoassay for the detection of fecal cortisol metabolites in several non domestic felid species. Proceedings of the American Association of Zoo Veterinarians; 1996 November 3-8; Puerto Vallarta, Mexico. St Louis Missouri USA: Charlotte Kirk editor, AZV-AZCARM: 1996: 582-583.
Sapolsky RM. Individual differences in cortisol secretory patterns in the wild baboon: role of negative feedback sensitivity. Endocrinology 1983; 113:2263-2267.
Friend TH, Polan CE, Gwazdauskas FC, Heald CW. Adrenal glucocorticoid response to exogenous adrenocorticotropin mediated by density and social disruption in lactating cows. J Dairy Sci 1977; 60:1958-1963.
Nogueira GP, Silva JCR. Plasma cortisol levels in captive wild felines after chemical restraint. Braz J Med Biol Res 1997; 30:1359-1361.
Morton DJ, Anderson E, Foggin CM, Kock MD, Tiran EP. Plasma cortisol as an indicator of stress due to capture and translocation in wildlife species. Vet Rec 1995; 136:60-63.
Brown JL, Goodrowe KL, Simmons LG, Armstrong DL, Wildt DE. Evaluation of the pituitary-gonadal response to GnRH, and adrenal status in the leopard (Panthera pardus japonensis) and tiger (Panthera tigris). J Reprod Fertil 1988; 82:227-236.
Aubin DJ, Ridgway SH, Wells RS, Rhinehart H. Dolphin thyroid and adrenal hormones: circulating levels in wild and semidomesticated Tursiops truncatus, and influence of sex, age and season. Marine Mammal Sci 1996; 12:1-13.
Parrot RF, Misson BH, Baldwin BA. Salivary cortisol in pigs following adrenocorticotrophic hormone stimulation: comparison with plasma levels. Br Vet J 1989; 145:362-366.
De Jong IC, Prelle IT, Van de Burgwal JA, Lambooij E, Korte SM, Blokhuis HJ, et al. Effects of environmental enrichment on behavioral responses to novelty, learning and memory, and the circadian rhythm in cortisol in growing pigs. Physiol Behav 2000; 68:571-578.
Lutz CK, Tiefenbacher S, Jorgensen MJ, Meyer JS, Novak MA. Techniques for collecting saliva from awake, unrestrained, adult rhesus monkeys for cortisol assay. Am J Primatol 2000; 52:93-99.
Hodges JK. Determining and manipulating female reproductive parameters. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S, editors. Wild mammals in captivity, principles and techniques. Chicago: The University of Chicago Press; 1996; 418-428.
Lasley, BL. Methods for evaluating reproductive function in exotic species. Adv Vet Sci Comp Med 1985; 30: 209-228.
Goossens MMC, Meyer HP, Voorhout G, Sprang EPM. Urinary excretion of glucocorticoids in the diagnosis of hyperadrenocorticism in cats. Dom Anim Endocrinol 1995; 12:355-362.
Korhonen H, Niemela P, Jauhiainen L, Tupasela T. Effects of space allowance and earthen floor on welfare-related physiological and behavioural responses in male blue foxes. Physiol Behav 2000; 69:571-580.
Crockett CM, Shimoji M, Bowden DM. Behavior, appetite and urinary cortisol responses by adult female pigtailed and longtailed macaques to cage size, cage level, room changes and sedation. Am J Primatol 2000; 52:63-80.
Carlstead K, Brown JL, Monfort SL, Killens R, Wildt DE. Urinary monitoring of adrenal responses to psychological stressors in domestic and nondomestic felids. Zoo Biol 1992; 11:165-176.
Bahr NI, Pryce CR, Dobeli M, Martin RD. Evidence from urinary cortisol that maternal behavior is related to stress in gorillas. Physiol Behav 1998; 64:429-437.
Carlstead K, Brown JL, Seidensticker J. Behavioral and adrenocortical responses to environmental changes in leopard cats (Felis bengalensis). Zoo Biol 1993; 12:321-331.
Palme R, Fischer P, Schildorfer H, Ismail MN: Excretion of infused 14C-steroid hormones via feces and urine in domestic livestock. Anim Reprod Sci 1996; 43:43-63.
Adams NR, Abordi JA, Briegel JR, Sanders MR. Effect of diet on the clearance of estradiol-17 in the ewe. Biol Reprod 1994; 51:668-674.
Wasser SK, Thomas R, Nair PP, Guidry C, Southers J, Lucas J, et al. Effects of dietary fiber on faecal steroid measurements in baboons (Papio cynocephalus cynocephalus). J Reprod Fertil 1993; 97:569-574.
McLeod PJ, Moger WH, Ryon J, Gadbois S, Fentress JC. The relation between urinary cortisol levels and social behavior in captive timber wolves. Can J Zool 1996; 74:209-216.
Morais, RN, Mucciolo RG, Gomes ML, Lacerda O, Moraes W, Moreira N, et al. Adrenal activity assessed by fecal corticoids and male reproductive traits in three South American felid species. Proceedings of the American Association of Zoo Veterinarians; 1996 November 3-8; Puerto Vallarta, Mexico. St Louis Missouri USA: Charlotte Kirk editor, AZV-AZCARM: 1996: 220-223.
Jurke MH, Czekala NM, Lindburg DG, Millard SE. Fecal corticoid metabolite measurement in the cheetah (Acinonyx jubatus). Zoo Biol 1997; 16:133-147.
Wallner B, Möstl E, Dittami J, Prossinger H. Fecal glucocorticoids document stress in female Barbary machaques (Macaca sylvanus). Gen Comp Endocrinol 1999; 113:80-86.
Möstl E, Palme R. Hormones as indicators of stress. Dom Anim Endocrinol 2002; 23:67-74
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